Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-29T00:53:05.508Z Has data issue: false hasContentIssue false

Does Colonization with Methicillin-Susceptible Staphylococcus aureus Protect against Nosocomial Acquisition of Methicillin-Resistant S. aureus?

Published online by Cambridge University Press:  10 May 2016

Caroline Landelle
Affiliation:
Infection Control Program, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Anne Iten
Affiliation:
Infection Control Program, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland Division of General Internal Medicine, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Ilker Uçkay
Affiliation:
Infection Control Program, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Hugo Sax
Affiliation:
Infection Control Program, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Véronique Camus
Affiliation:
Infection Control Program, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Gilles Cohen
Affiliation:
Division of Medico-Economic Analysis, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Gesuele Renzi
Affiliation:
Clinical Microbiology Laboratory, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Jacques Schrenzel
Affiliation:
Clinical Microbiology Laboratory, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Didier Pittet
Affiliation:
Infection Control Program, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Arnaud Perrier
Affiliation:
Division of General Internal Medicine, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Stephan Harbarth*
Affiliation:
Infection Control Program, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
*
Infection Control Program, University of Geneva Hospitals and Medical School, 4 Rue Gabrielle Perret-Gentil, 1211 Geneva 14, Switzerland ([email protected])

Abstract

Objective.

To test the hypothesis that methicillin-susceptible Staphylococcus aureus (MSSA) carriage may protect against nosocomial methicillin-resistant S. aureus (MRSA) acquisition by competing for colonization of the anterior nares.

Design.

Prospective cohort and nested case-control study.

Setting.

Swiss university hospital.

Patients.

All adult patients admitted to 14 wards of the general medicine division between April 1 and October 31, 2007.

Methods.

Patients were screened for MRSA and MSSA carriage at admission to and discharge from the division. Associations between nosocomial MRSA acquisition and MSSA colonization at admission and other confounders were analyzed by univariable and multivariable analysis.

Results.

Of 898 patients included, 183 (20%) were treated with antibiotics. Nosocomial MRSA acquisition occurred in 70 (8%) of the patients (case patients); 828 (92%) of the patients (control subjects) were free of MRSA colonization at discharge. MSSA carriage at admission was 20% and 21% for case patients and control subjects, respectively. After adjustment by multivariate logistic regression, no association was observed between MSSA colonization at admission and nosocomial MRSA acquisition (adjusted odds ratio [aOR], 1.2 [95% confidence interval (CI), 0.6–2.3]). By contrast, 4 independent predictors of nosocomial MRSA acquisition were identified: older age (aOR per 1-year increment, 1.05 [95% CI, 1.02–1.08]); increased length of stay (aOR per 1-day increment, 1.05 [95% CI, 1.02–1.09]); increased nursing workload index (aOR per 1-point increment, 1.02 [95% CI, 1.01–1.04]); and previous treatment with macrolides (aOR, 5.6 [95% CI, 1.8–17.7]).

Conclusions.

Endogenous MSSA colonization does not appear to protect against nosocomial MRSA acquisition in a population of medical patients without frequent antibiotic exposure.

Type
Original Article
Copyright
Copyright © The Society for Healthcare Epidemiology of America 2014

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a.

C.L. and A.I. contributed equally to this study.

References

1. Lepelletier, D, Lucet, JC. Controlling meticillin-susceptible Staphylococcus aureus: not simply meticillin-resistant S. aureus revisited. J Hosp Infect 2013;84:1321.CrossRefGoogle Scholar
2. Wertheim, HF, Melles, DC, Vos, MC, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 2005;5:751762.Google Scholar
3. den Heijer, CD, van Bijnen, EM, Paget, WJ, et al. Prevalence and resistance of commensal Staphylococcus aureus, including meticillin-resistant S. aureus, in nine European countries: a cross-sectional study. Lancet Infect Dis 2013;13:409415.CrossRefGoogle ScholarPubMed
4. Harbarth, S, Sax, H, Fankhauser-Rodriguez, C, Schrenzel, J, Agos-tinho, A, Pittet, D. Evaluating the probability of previously unknown carriage of MRSA at hospital admission. Am J Med 2006;119:275.e15e23.CrossRefGoogle ScholarPubMed
5. Harbarth, S, Fankhauser, C, Schrenzel, J, et al. Universal screening for methicillin-resistant Staphylococcus aureus at hospital admission and nosocomial infection in surgical patients. JAMA 2008;299:11491157.CrossRefGoogle ScholarPubMed
6. Jain, R, Kralovic, SM, Evans, ME, et al. Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections. N Engl J Med 2011;364:14191430.CrossRefGoogle ScholarPubMed
7. Furuno, JP, McGregor, JC, Harris, AD, et al. Identifying groups at high risk for carriage of antibiotic-resistant bacteria. Arch Intern Med 2006;166:580585.Google Scholar
8. Asensio, A, Guerrero, A, Quereda, C, Lizan, M, Martinez-Ferrer, M. Colonization and infection with methicillin-resistant Staphylococcus aureus: associated factors and eradication. Infect Control Hosp Epidemiol 1996;17:2028.Google Scholar
9. Coello, R, Glynn, JR, Gaspar, C, Picazo, JJ, Fereres, J. Risk factors for developing clinical infection with methicillin-resistant Staphylococcus aureus (MRSA) amongst hospital patients initially only colonized with MRSA. J Hosp Infect 1997;37:3946.CrossRefGoogle ScholarPubMed
10. Pujol, M, Pena, C, Pallares, R, Ayats, J, Ariza, J, Gudiol, F. Risk factors for nosocomial bacteremia due to methicillin-resistant Staphylococcus aureus . Eur J Clin Microbiol Infect Dis 1994;13:96102.Google Scholar
11. Pujol, M, Pena, C, Pallares, R, et al. Nosocomial Staphylococcus aureus bacteremia among nasal carriers of methicillin-resistant and methicillin-susceptible strains. Am J Med 1996;100:509516.CrossRefGoogle ScholarPubMed
12. Safdar, N, Bradley, EA. The risk of infection after nasal colonization with Staphylococcus aureus . Am J Med 2008;121:310315.CrossRefGoogle ScholarPubMed
13. Graffunder, EM, Venezia, RA. Risk factors associated with nosocomial methicillin-resistant Staphylococcus aureus (MRSA) infection including previous use of antimicrobials. J Antimicrob Chemother 2002;49:9991005.CrossRefGoogle ScholarPubMed
14. Salangsang, JA, Harrison, LH, Brooks, MM, Shutt, KA, Saul, MI, Muto, CA. Patient-associated risk factors for acquisition of methicillin-resistant Staphylococcus aureus in a tertiary care hospital. Infect Control Hosp Epidemiol 2010;31:11391147.CrossRefGoogle ScholarPubMed
15. Marshall, C, Harrington, G, Wolfe, R, Fairley, CK, Wesselingh, S, Spelman, D. Acquisition of methicillin-resistant Staphylococcus aureus in a large intensive care unit. Infect Control Hosp Epidemiol 2003;24:322326.CrossRefGoogle Scholar
16. Dall'Antonia, M, Coen, PG, Wilks, M, Whiley, A, Millar, M. Competition between methicillin-sensitive and -resistant Staphylococcus aureus in the anterior nares. J Hosp Infect 2005;61:6267.Google Scholar
17. Huang, SS, Datta, R, Rifas-Shiman, S, et al. Colonization with antibiotic-susceptible strains protects against methicillin-resistant Staphylococcus aureus but not vancomycin-resistant enter-ococci acquisition: a nested case-control study. Crit Care 2011;15:R210.Google Scholar
18. Krebes, J, Al-Ghusein, H, Feasey, N, Breathnach, A, Lindsay, JA. Are nasal carriers of Staphylococcus aureus more likely to become colonized or infected with methicillin-resistant Staphylococcus aureus on admission to a hospital? J Clin Microbiol 2011;49:430432.CrossRefGoogle ScholarPubMed
19. Pasricha, J, Harbarth, S, Koessler, T, et al. Methicillin-resistant Staphylococcus aureus risk profiling: who are we missing? Antimicrob Resist Infect Control 2013;2:17.Google Scholar
20. Sax, H, Allegranzi, B, Uckay, I, Larson, E, Boyce, J, Pittet, D. “My five moments for hand hygiene”: a user-centred design approach to understand, train, monitor and report hand hygiene. J Hosp Infect 2007;67:921.CrossRefGoogle ScholarPubMed
21. Pittet, D, Safran, E, Harbarth, S, et al. Automatic alerts for methicillin-resistant Staphylococcus aureus surveillance and control: role of a hospital information system. Infect Control Hosp Epidemiol 1996;17:496502.CrossRefGoogle ScholarPubMed
22. Francois, P, Pittet, D, Bento, M, et al. Rapid detection of methicillin-resistant Staphylococcus aureus directly from sterile or nonsterile clinical samples by a new molecular assay. J Clin Microbiol 2003;41:254260.Google Scholar
23. Saulnier, FF, Hubert, H, Onimus, TM, et al. Assessing excess nurse work load generated by multiresistant nosocomial bacteria in intensive care. Infect Control Hosp Epidemiol 2001;22:273278.CrossRefGoogle ScholarPubMed
24. Quan, H, Li, B, Couris, CM, et al. Updating and validating the Charlson comorbidity index and score for risk adjustment in hospital discharge abstracts using data from 6 countries. Am J Epidemiol 2011;173:676682.CrossRefGoogle ScholarPubMed
25. Pasricha, J, Koessler, T, Harbarth, S, et al. Carriage of extended-spectrum beta-lactamase-producing enterobacteriacae among internal medicine patients in Switzerland. Antimicrob Resist Infect Control 2013;2:20.Google Scholar
26. Shinefield, HR, Wilsey, JD, Ribble, JC, Boris, M, Eichenwald, HF, Dittmar, CI. Interactions of staphylococcal colonization. Influence of normal nasal flora and antimicrobials on inoculated Staphylococcus aureus strain 502A. Am J Dis Child 1966;111:1121.Google Scholar
27. Strauss, WG, Maibach, HI, Shinefield, HR. Bacterial interference treatment of recurrent furunculosis. 2. Demonstration of the relationship of strain to pathogeneicity. JAMA 1969;208:861863.Google Scholar
28. Lucet, JC, Paoletti, X, Lolom, I, et al. Successful long-term program for controlling methicillin-resistant Staphylococcus aureus in intensive care units. Intensive Care Med 2005;31:10511057.Google Scholar
29. Fishbain, JT, Lee, JC, Nguyen, HD, et al. Nosocomial transmission of methicillin-resistant Staphylococcus aureus: a blinded study to establish baseline acquisition rates. Infect Control Hosp Epidemiol 2003;24:415421.CrossRefGoogle ScholarPubMed
30. Ho, PL. Carriage of methicillin-resistant Staphylococcus aureus, ceftazidime-resistant gram-negative bacilli, and vancomycin-resistant enterococci before and after intensive care unit admission. Crit Care Med 2003;31:11751182.Google Scholar
31. Vernaz, N, Sax, H, Pittet, D, Bonnabry, P, Schrenzel, J, Harbarth, S. Temporal effects of antibiotic use and hand rub consumption on the incidence of MRSA and Clostridium difficile . J Antimicrob Chemother 2008;62:601607.Google Scholar
32. Tacconelli, E, De Angelis, G, Cataldo, MA, Pozzi, E, Cauda, R. Does antibiotic exposure increase the risk of methicillin-resistant Staphylococcus aureus (MRSA) isolation? a systematic review and meta-analysis. J Antimicrob Chemother 2008;61:2638.Google Scholar
33. Hugonnet, S, Harbarth, S, Sax, H, Duncan, RA, Pittet, D. Nursing resources: a major determinant of nosocomial infection? Curr Opin Infect Dis 2004;17:329333.Google Scholar
34. Harbarth, S, Sudre, P, Dharan, S, Cadenas, M, Pittet, D. Outbreak of Enterobacter cloacae related to understaffmg, overcrowding, and poor hygiene practices. Infect Control Hosp Epidemiol 1999;20 598603.Google Scholar
35. Kluytmans, J, van Belkum, A, Verbrugh, H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 1997;10:505520.Google Scholar
36. Huttner, A, Von Dach, E, Liassine, N, et al. Surveillance and control of community-associated methicillin-resistant Staphylococcus aureus in Geneva, Switzerland, 2002–2012. Antimicrob Resist Infect Control 2013;2:P60.Google Scholar
37. De Angelis, G, Francois, P, Lee, A, et al. Molecular and epidemiological evaluation of strain replacement in patients previously harboring gentamicin-resistant MRSA. J Clin Microbiol 2011;49:38803884.Google Scholar
38. Ajao, AO, Harris, AD, Roghmann, MC, et al. Systematic review of measurement and adjustment for colonization pressure in studies of methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci, and Clostridium difficile acquisition. Infect Control Hosp Epidemiol 2011;32:481489.CrossRefGoogle ScholarPubMed
39. Acton, DS, Plat-Sinnige, MJ, van Wamel, W, de Groot, N, van Belkum, A. Intestinal carriage of Staphylococcus aureus: how does its frequency compare with that of nasal carriage and what is its clinical impact? Eur J Clin Microbiol Infect Dis 2009;28:115127.Google Scholar
40. Sanford, MD, Widmer, AF, Bale, MJ, Jones, RN, Wenzel, RP Efficient detection and long-term persistence of the carriage of methicillin-resistant Staphylococcus aureus . Clin Infect Dis 1994; 19 11231128.Google Scholar
41. Harbarth, S, Schrenzel, J, Renzi, G, Akakpo, C, Ricou, B. Is throat screening necessary to detect methicillin-resistant Staphylococcus aureus colonization in patients upon admission to an intensive care unit? J Clin Microbiol 2007;45:10721073.CrossRefGoogle Scholar